Dynamic changes in E-protein activity regulate T reg cell development

Journal of Experimental Medicine

Volumn 211, Issue 13, 2014, Pages 2651-2668

  Gao, Ping ^a   Han, Xiaojuan ^a   Zhang, Qi ^a   Yang, Zhiqiong ^b   Fuss, Ivan J ^b   Myers, Timothy G ^b   Gardina, Paul J ^b   Zhang, Fuping ^a   Strober, Warren ^b  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

E PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF DIFFERENTIATION PROTEIN; INTERLEUKIN 2 RECEPTOR; NUCLEAR RECEPTOR NUR77; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CD4 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; LYMPHOCYTE ANTIGEN RECEPTOR; STAT5 PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; DOWN REGULATION; GENE LOCUS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; THYMUS; ANIMAL; CYTOLOGY; DNA MICROARRAY; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; ANTIGENS, CD4; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; FORKHEAD TRANSCRIPTION FACTORS; GENE DELETION; GENE EXPRESSION REGULATION; INHIBITOR OF DIFFERENTIATION PROTEINS; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE, KNOCKOUT; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND; TRANSCRIPTION, GENETIC;

EID: 84930834791     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20132681     Document Type: Article

References (35)

1. Bayer, A.L., A. Yu, and T.R. Malek. 2007. Function of the IL-2R for thymic and peripheral CD4+CD25+ Foxp3+ T regulatory cells. J. Immunol. 178:4062-4071. http://dx.doi.org/10.4049/jimmunol.178.7.4062
2. Bellavia, D., A.F. Campese, E. Alesse, A. Vacca, M.P. Felli, A. Balestri, A. Stoppacciaro, C. Tiveron, L. Tatangelo, M. Giovarelli, et al. 2000. Constitutive activation of NF-kappaB and T-cell leukemia/lymphoma in Notch3 transgenic mice. EMBO J. 19:3337-3348. http://dx.doi.org/10.1093/emboj/19.13.3337
3. Burchill, M.A., J. Yang, C. Vogtenhuber, B.R. Blazar, and M.A. Farrar. 2007. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells. J. Immunol. 178:280-290. http://dx.doi.org/10.4049/jimmunol.178.1.280
4. Burchill, M.A., J. Yang, K.B. Vang, J.J. Moon, H.H. Chu, C.W. Lio, A.L. Vegoe, C.S. Hsieh, M.K. Jenkins, and M.A. Farrar. 2008. Linked T cell receptor and cytokine signaling govern the development of the regulatory T cell repertoire. Immunity. 28:112-121. http://dx.doi.org/10.1016/j.immuni.2007.11.022
5. Cheng, G., A. Yu, and T.R. Malek. 2011. T-cell tolerance and the multifunctional role of IL-2R signaling in T-regulatory cells. Immunol. Rev. 241:63-76. http://dx.doi.org/10.1111/j.1600-065X.2011.01004.x
6. Engel, I., C. Johns, G. Bain, R.R. Rivera, and C. Murre. 2001. Early thymocyte development is regulated by modulation of E2A protein activity. J. Exp. Med. 194:733-745. http://dx.doi.org/10.1084/jem.194.6.733
7. Gupta, S., S. Manicassamy, C. Vasu, A. Kumar, W. Shang, and Z. Sun. 2008. Differential requirement of PKC-theta in the development and function of natural regulatory T cells. Mol. Immunol. 46:213-224. http://dx.doi.org/10.1016/j.molimm.2008.08.275
8. Hill, J.A., M. Feuerer, K. Tash, S. Haxhinasto, J. Perez, R. Melamed, D. Mathis, and C. Benoist. 2007. Foxp3 transcription-factor-dependent and -independent regulation of the regulatory T cell transcriptional signature. Immunity. 27:786-800. http://dx.doi.org/10.1016/j.immuni.2007.09.010
9. Hsieh, C.S., H.M. Lee, and C.W. Lio. 2012. Selection of regulatory T cells in the thymus. Nat. Rev. Immunol. 12:157-167.
10. Isomura, I., S. Palmer, R.J. Grumont, K. Bunting, G. Hoyne, N. Wilkinson, A. Banerjee, A. Proietto, R. Gugasyan, L. Wu, et al. 2009. c-Rel is required for the development of thymic Foxp3+ CD4 regulatory T cells. J. Exp. Med. 206:3001-3014. http://dx.doi.org/10.1084/jem.20091411
11. Jones, M.E., and Y. Zhuang. 2007. Acquisition of a functional T cell receptor during T lymphocyte development is enforced by HEB and E2A transcription factors. Immunity. 27:860-870. http://dx.doi.org/10.1016/j.immuni.2007.10.014
12. Jones, M.E., and Y. Zhuang. 2011. Stage-specific functions of E-proteins at the β-selection and T-cell receptor checkpoints during thymocyte development. Immunol. Res. 49:202-215. http://dx.doi.org/10.1007/s12026-010-8182-x
13. Jones, M.E., M. Kondo, and Y. Zhuang. 2009. A tamoxifen inducible knock-in allele for investigation of E2A function. BMC Dev. Biol. 9:51. http://dx.doi.org/10.1186/1471-213X-9-51
14. Jones-Mason, M.E., X. Zhao, D. Kappes, A. Lasorella, A. Iavarone, and Y. Zhuang. 2012. E protein transcription factors are required for the development of CD4(+) lineage T cells. Immunity. 36:348-361. http://dx.doi.org/10.1016/j.immuni.2012.02.010
15. Kanno, Y., Y. Takane, Y. Takizawa, and Y. Inouye. 2008. Suppressive effect of aryl hydrocarbon receptor repressor on transcriptional activity of estrogen receptor alpha by protein-protein interaction in stably and transiently expressing cell lines. Mol. Cell. Endocrinol. 291:87-94. http://dx.doi.org/10.1016/j.mce.2008.05.004
16. Kee, B.L. 2009. E and ID proteins branch out. Nat. Rev. Immunol. 9:175-184. http://dx.doi.org/10.1038/nri2507
17. Kim, D., M. Xu, L. Nie, X.C. Peng, E. Jimi, R.E. Voll, T. Nguyen, S. Ghosh, and X.H. Sun. 2002. Helix-loop-helix proteins regulate pre-TCR and TCR signaling through modulation of Rel/NF-kappaB activities. Immunity. 16:9-21. http://dx.doi.org/10.1016/S1074-7613(02)00264-9
18. Lio, C.W., and C.S. Hsieh. 2008. A two-step process for thymic regulatory T cell development. Immunity. 28:100-111. http://dx.doi.org/10.1016/j.immuni.2007.11.021
19. Long, M., S.G. Park, I. Strickland, M.S. Hayden, and S. Ghosh. 2009. Nuclear factor-kappaB modulates regulatory T cell development by directly regulating expression of Foxp3 transcription factor. Immunity. 31:921-931. http://dx.doi.org/10.1016/j.immuni.2009.09.022
20. Malek, T.R. 2008. The biology of interleukin-2. Annu. Rev. Immunol. 26:453-479. http://dx.doi.org/10.1146/annurev.immunol.26.021607.090357
21. Maruyama, T., J. Li, J.P. Vaque, J.E. Konkel, W. Wang, B. Zhang, P. Zhang, B.F. Zamarron, D. Yu, Y. Wu, et al. 2011. Control of the differentiation of regulatory T cells and T(H)17 cells by the DNA-binding inhibitor Id3. Nat. Immunol. 12:86-95. http://dx.doi.org/10.1038/ni.1965
22. Medoff, B.D., B.P. Sandall, A. Landry, K. Nagahama, A. Mizoguchi, A.D. Luster, and R.J. Xavier. 2009. Differential requirement for CARMA1 in agonist-selected T-cell development. Eur. J. Immunol. 39:78-84. http://dx.doi.org/10.1002/eji.200838734
23. Miyazaki, M., K. Miyazaki, S. Chen, M. Itoi, M. Miller, L.F. Lu, N. Varki, A.N. Chang, D.H. Broide, and C. Murre. 2014. Id2 and Id3 maintain the regulatory T cell pool to suppress inflammatory disease. Nat. Immunol. 15:767-776. http://dx.doi.org/10.1038/ni.2928
24. Moran, A.E., K.L. Holzapfel, Y. Xing, N.R. Cunningham, J.S. Maltzman, J. Punt, and K.A. Hogquist. 2011. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 208:1279-1289. http://dx.doi.org/10.1084/jem.20110308
25. Murre, C. 2005. Helix-loop-helix proteins and lymphocyte development. Nat. Immunol. 6:1079-1086. http://dx.doi.org/10.1038/ni1260
26. Ruan, Q., V. Kameswaran, Y. Tone, L. Li, H.C. Liou, M.I. Greene, M. Tone, and Y.H. Chen. 2009. Development of Foxp3(+) regulatory t cells is driven by the c-Rel enhanceosome. Immunity. 31:932-940. http://dx.doi.org/10.1016/j.immuni.2009.10.006
27. Schwartz, R., I. Engel, M. Fallahi-Sichani, H.T. Petrie, and C. Murre. 2006. Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development. Proc. Natl. Acad. Sci. USA. 103:9976-9981. http://dx.doi.org/10.1073/pnas.0603728103
28. Vang, K.B., J. Yang, S.A. Mahmud, M.A. Burchill, A.L. Vegoe, and M.A. Farrar. 2008. IL-2, -7, and -15, but not thymic stromal lymphopoeitin, redundantly govern CD4+Foxp3+ regulatory T cell development. J. Immunol. 181:3285-3290. http://dx.doi.org/10.4049/jimmunol.181.5.3285
29. Vang, K.B., J. Yang, A.J. Pagán, L.X. Li, J. Wang, J.M. Green, A.A. Beg, and M.A. Farrar. 2010. Cutting edge: CD28 and c-Rel-dependent pathways initiate regulatory T cell development. J. Immunol. 184:4074-4077. http://dx.doi.org/10.4049/jimmunol.0903933
30. Verykokakis, M., M.D. Boos, A. Bendelac, and B.L. Kee. 2010. SAP protein-dependent natural killer T-like cells regulate the development of CD8(+) T cells with innate lymphocyte characteristics. Immunity. 33:203-215. http://dx.doi.org/10.1016/j.immuni.2010.07.013
31. Yang, Y., H.C. Liou, and X.H. Sun. 2006. Id1 potentiates NF-kappaB activation upon T cell receptor signaling. J. Biol. Chem. 281:34989-34996. http://dx.doi.org/10.1074/jbc. M608078200
32. Yao, Z., Y. Kanno, M. Kerenyi, G. Stephens, L. Durant, W.T. Watford, A. Laurence, G.W. Robinson, E.M. Shevach, R. Moriggl, et al. 2007. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood. 109:4368-4375. http://dx.doi.org/10.1182/blood-2006-11-055756
33. Zhang, F., G. Meng, and W. Strober. 2008. Interactions among the transcription factors Runx1, RORgammat and Foxp3 regulate the differentiation of interleukin 17-producing T cells. Nat. Immunol. 9:1297-1306. http://dx.doi.org/10.1038/ni.1663
34. Zhang, B., Y.Y. Lin, M. Dai, and Y. Zhuang. 2014. Id3 and Id2 act as a dual safety mechanism in regulating the development and population size of innate-like γδ T cells. J. Immunol. 192:1055-1063. http://dx.doi.org/10.4049/jimmunol.1302694
35. Zheng, Y., S. Josefowicz, A. Chaudhry, X.P. Peng, K. Forbush, and A.Y. Rudensky. 2010. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature. 463:808-812. http://dx.doi.org/10.1038/nature08750